Comments on Doguet et al. (2017) ‘Muscle length effect on corticospinal excitability during maximal concentric, isometric and eccentric contractions of the knee extensors’

In their recent paper, Doguet et al. (2017) investigated the influence of muscle length on corticospinal excitability of the vastus lateralis during concentric, isometric and eccentric contraction types. From their study, the authors drew the following two main conclusions: (i) corticospinal excitability during maximal voluntary eccentric contractions of the knee-extensor muscles was influenced by muscle length; and (ii) neural control of eccentric contractions differed from that during concentric and isometric contractions. Although the authors address an important issue regarding our understanding of the neural control of eccentric contractions, several conceptual and methodological shortcomings common to this field of research raise concerns about the conclusions drawn by Doguet et al. (2017). The central aim of the study by Doguet et al. (2017) was to investigate whether corticospinal excitability is affected by muscle length during eccentric contractions. Accordingly, muscle length should be isolated as an independent variable during the experiment. However, in the study by Doguet et al. (2017) there are several confounding variables that could have affected their interpretation of the results. Basically, theses confounders arise from two conceptual aspects. Firstly, the eccentric contractions were performed over a 70 deg range of motion, from 40 to 110 deg knee flexion, whereas corticospinal excitability was evaluated at two predefined target knee-flexion angles of 75 and 100 deg, which were chosen to represent intermediate and long muscle lengths, respectively. Therefore, the range of motion (and the time under tension) to reach the target angles was not fixed during the eccentric contractions. Secondly, a major methodological shortcoming was that Doguet et al. (2017) did not account for variable muscle fascicle behaviour during the eccentric contractions over the given range of motion, which is complicated by series elasticity within the intact muscle–tendon unit (MTU). At the beginning of their paper, the authors define the lengthening of an MTU as an eccentric contraction, but neglect the finding that muscle fascicles have been shown to remain isometric or even shorten during lengthening of a relatively compliant MTU, such as the cat medial gastrocnemius (Griffiths, 1991). This MTU has a similar tendon-to-fibre length ratio (5:1) to the human quadriceps MTUs (3–5:1; Zajac, 1989), which suggests that a similar behaviour could occur in the knee extensors during MTU stretch. As differences in muscle–tendon interaction between the contraction types and at the two different muscle lengths were not assessed by Doguet et al. (2017), this complicates the interpretation of their results. Although it might be safe to assume that there was fascicle stretch in the vastus lateralis muscle over the 70 deg knee joint rotation, the fascicle stretch amplitude and fascicle velocity are likely to have differed during the same eccentric contraction when compared at the intermediate and long muscle lengths. Therefore, there are at least four independent variables (fascicle length, fascicle stretch amplitude, fascicle velocity and time under tension) that might also explain the changes in corticospinal excitability during the eccentric contractions at the intermediate and long muscle lengths. Accordingly, the observed modulations in corticospinal excitability across the contraction types can hardly be attributed solely to muscle length. The second main finding of the study by Doguet et al. (2017) was that neural control in eccentric contractions differs from that in concentric and isometric contractions. Again, there are several problems with this conclusion. Firstly, participants were not familiarized with the eccentric contractions, and these were performed after the concentric and isometric contractions, in order to avoid muscle damage from confounding their results across the contraction types. However, muscle damage might have occurred in the first eccentric contraction, which could have resulted in muscle damage confounding the results from the remaining 11 eccentric contractions. Accordingly, the neurophysiological measurements from the eccentric contractions and their interpretation are potentially biased by muscle damage. Secondly, fatigue is likely to be an additional confounder, because the torque from the first to the last eccentric contractions at the long muscle length decreased significantly. A simple familiarization session before the experiment would have been likely to eliminate these two confounding variables, because the repeated bout effect could have been leveraged to prevent muscle damage in the experimental session and thus permit the randomization of each contraction. Thirdly, when comparing the neural control during eccentric, concentric and isometric contractions, Doguet et al. (2017) again did not account for fascicle behaviour. However, owing to the series elasticity within an MTU, identical knee-joint angles do not guarantee identical fascicle lengths (see fig. 2 of Hahn, 2018), which complicates the interpretation of the results obtained by Doguet et al. (2017). Another major limitation not discussed by Doguet et al. (2017) was that, according to their table 1, eccentric torques did not exceed, but were similar to the corresponding isometric reference torques. Although this was reported in several other studies in the field, at least me this is surprising, because significantly increased torques during eccentric contractions compared with isometric contractions have previously been shown in voluntarily activated knee-extensor muscles (Hahn, Seiberl, & Schwirtz, 2007). Thus, doubt arises as to whether the participants were able to perform truly maximal voluntary eccentric contractions. Again, this might have biased the interpretation of the measurements obtained by transcranial magnetic stimulation, for the following reasons. Considering that eccentric torques were similar to the isometric torques at the intermediate and long muscle lengths, the EMG level was likely to be lower during the eccentric contractions, too. This is because eccentric torque production can be attributable to stretch of passive elastic structures that do not require activation. However, given that motor evoked potentials after transcranial magnetic stimulation depend on the background activation level, the main finding of different neural control during eccentric contractions might simply be attributable to changes in activation level. Unfortunately, no quantitative information on background EMG levels is provided during the different contraction types in the paper by Doguet et al. (2017). However, according to individual data from their fig. 1, it seems that muscle activity during the eccentric contractions was indeed lower, at least compared with the concentric contractions. In summary, the modulation of corticospinal excitability as observed by Doguet et al. (2017) cannot be attributed solely to differences in muscle length and contraction type. As fascicle behaviour was not measured and given that the participants failed to produce eccentric torques that exceeded their isometric force capacity, it remains unclear whether the neural control during eccentric contractions truly differs compared with isometric and concentric contractions, or if the findings are attributable to different fascicle mechanics and/or that participants were simply unable to perform maximal voluntary eccentric contractions because of muscle damage or fatigue or a lack of familiarization. Thus, this letter to the editor will hopefully motivate the authors to revisit their study with an improved methodology and design that includes ultrasound imaging to determine muscle fascicle behaviour and also implement randomized and truly maximal contractions. Overall, I think it is far less clear than suggested in the literature that neural control during eccentric contractions is truly unique compared with isometric and concentric contraction types (Hahn, 2018). I thank Dr Brent Raiteri for critically revising and proofreading this manuscript. None declared.